Human. Part 5

If you can come up with some reasonable answers that satisfy you, consider this one last phenomenon. Patient X, who has suffered a stroke, has this condition. His eyes can still take in visual stimuli, but the primary part of his visual cortex has been destroyed. He is blind. He cannot even distinguish light from dark. You can show him pictures of circles or squares, or ask him to distinguish between photos of men or women, and he has no idea what is in front of him. You can show him snarling animal faces or calm animal faces, and he has nothing to say, but if you show him pictures of angry or happy human faces, he, like some other patients with this kind of brain lesion, can guess what the emotions are.1 He has what has come to be called blindsight.

How do we recognize the emotional states of others? Is it a conscious appraisal, or is it automatic? There are a few schools of thought about this. One school holds that an individual uses her own version of psychology, which is either innate or learned, and infers the mental state of others from how they are acting and what they are doing, where they are and whom they are with, and how they have been in the past. This is called theory theory. The other school holds that one infers another's emotional state by deliberately and voluntarily attempting to simulate or replicate it in one's own mind-first pretending to be in the other's situation and seeing how that feels, then feeding that information to the decision-making process, and ending up with what one thinks the other is feeling. This is called simulation theory.2 Both of these theories are volitional. You actually decide to evaluate the other's emotional state. Neither of them can explain patient X's ability to determine emotions.

In another form of the simulation theory, the simulation is not deliberate and voluntary but automatic and involuntary.3 In other words, it just happens without your control or rational input. You perceive an emotional stimulus through your senses, and your body automatically responds to it by simulating the emotion, which your conscious mind can either recognize or not. This could help us explain patient X. And of course there is the combo theory, which is part theory theory and part simulation theory, part automatic and part volitional. A lot of the controversy, as usual, seems to be about how much is automatic, or voluntary, or a learned response. Because our social interactions are vastly important to being human, and because recognizing the states of mind, emotions, and intentions of others is necessary to interact, how this all comes about is extremely intriguing as well as controversial.

There is also the question of empathy, and understanding why some individuals use it selectively or lack it altogether. Other social animals share at least some of our capabilities, but is there something unique going on in our brains that allows us to have more complex interactions? Much evidence is acc.u.mulating that we automatically simulate the internal experiences of others, and that this simulation contributes to empathy and theory of mind. Is it all automatic, or does the conscious brain contribute to such evaluations? Let's see what has been discovered so far.

VOLUNTARY SIMULATION: PHYSICAL IMITATION.

About thirty years ago, the field of child development got a shock. Up until that time, it had been thought that when babies imitate a motor movement, it was learned. The theory was that the visual perception of a movement and the execution of the imitative movement by the motor system were independent of each other and controlled by different parts of the brain. Then a study of imitative behavior of young infants done by University of Washington psychologists Andrew Meltzoff and M. Keith Moore suggested perhaps the visual perception of a motor movement (such as tongue protrusion or lip smacking) and the production of the movement (actually copying the movement) were not separately acquired abilities but were linked somehow.4 Since then, many independent studies5 have shown that newborns from the age of forty-two minutes to seventy-two hours can imitate facial expressions accurately.6, 7 Think about it. One can only be amazed what the brain is doing when it is less than one hour old. It sees there is a face with a tongue sticking out, somehow knows it too has a face with a tongue under its command, decides it will imitate the action, finds the tongue in its long list of body parts, gives it a little test run, commands it to be stuck out-and out it goes. How does she know a tongue is a tongue? How does she know what neural system is in charge of the tongue, and how does she know how to move it? Why does she even bother doing it? Obviously, it was not learned by looking in a mirror, nor had anyone taught it to her. The ability to imitate must be innate.8 Imitation is the beginning of a baby's social interaction. Babies will imitate human actions, but not those of objects; they understand they are like other people.9 The brain has specific neural circuits for identifying biological motion and inanimate object motion, along with specific circuits to identify faces and facial movement.10 What can a baby do to enter the social world before it can sit up or control its head or talk? How can she engage another person and form a social link? When you first hold a baby, what links her to you and you to her are her imitative actions. You stick out your tongue, she sticks out her tongue; you purse your lips, she purses her lips. She doesn't lie there like an object but responds in a way that you can relate to. In fact it has been shown that infants use imitation games to check the ident.i.ty of persons, and do not use only their facial features.11, 12 After about three months of age, this type of imitation can no longer be elicited. Imitative abilities then develop that show that the infant understands the meaning of what is being copied: The imitative movements don't have to be exact but are directed toward a goal. The infant puts the sand in the bucket, but the fingers on the shovel don't have to be held in exactly the same way as the fingers of the person showing her how to use the shovel; the goal is getting the sand in the bucket. We have all seen how young children play when they are together, so it comes as no surprise that children aged eighteen to thirty months use imitation in their social exchanges, take turns between being the imitator and the imitatee, share topics, and in short, use imitation as communication.13 Imitating others is a potent mechanism in learning and acculturation.14 Voluntary behavior imitation appears to be rare in the animal kingdom. No evidence of voluntary imitation by monkeys, regardless of how many years they have been trained,15, 16 has been reported, except in one study in which imitative behavior was elicited in two j.a.panese monkeys who were so highly trained that they had learned to follow the eye gaze of a human.17 So much for "monkey see, monkey do." To what extent voluntary imitation exists in other animals is controversial. It depends on the definition of imitation and how many other factors are involved, a few of which are whether the imitation is goal directed, exact, motivated, social, or learned.18 It appears to exist to some degree in the great apes and some birds, and there is some evidence that it is present in cetaceans.19 The fact that many people are watching for and testing for imitation in the animal world but have found little evidence of it, and the fact that when it has been found, it has been of limited scope, indicate that the ubiquitious and extensive imitation in the human world is very different.

INVOLUNTARY PHYSICAL IMITATION: MIMICRY.

There is a difference between active imitation and what is known as mimicry, which is nonconscious imitation. In the last chapter, we learned a bit about nonconscious mimicry from the research done by John Bargh at New York University. People will unconsciously copy mannerisms of others, and not only will they not know they are doing it, but they will not consciously realize the other person even has a mannerism they could be mimicking. That is not all. We are virtual mimicking machines! People will not only mimic mannerisms but also unconsciously mimic the facial expressions, postures, vocal intonations, accents,20 and even speech patterns and words of others.21 How often have you noticed when you telephone a friend that their relative or their roommate who answers the phone sounds like your friend? Or how about all those married couples who start looking alike?

Our faces are our most prominent social feature, and they reflect our emotional states, but they also react to the emotional states of others. This can happen so fast that you are not aware of either the other person's expression or that you have had a reaction. In one experiment, subjects were shown thirty-millisecond exposures of happy, neutral, and angry faces. This is too fast for them to consciously realize that a face was seen. This image was immediately followed by pictures of neutral faces. Even though the exposure to happy and angry faces was unconscious, the subjects reacted with distinct facial muscle reactions that corresponded to the happy and angry faces. Their facial muscular activity was measured by electromyography. Both positive and negative emotional reactions were unconsciously evoked; this demonstrates that some emotional face-to-face communication occurs on an unconscious level.22 People will also mimic body movements during conversation. One researcher videotaped a series of sessions in which she told a group of subjects about how she had to duck to avoid being run into at a party and demonstrated by ducking to the right. The video revealed that as they were listening, the listeners mimicked her movements and had strongly tended to duck to the left-the mirror image of her movement.23 Have you ever noticed that your own speech pattern may change when you are visiting different parts of the country or other countries? Partners in conversations will tend to match each other in rhythm of speech, length of pauses, and likelihood of breaking silences.24 All this is going on without your consciously willing it to happen. What's the point?

All this mimicking behavior greases the machinery of social interactions. Unconsciously, deep down in that automatic part of your brain, you form connections with, and you like, other people who are similar to you. Think how often you have said, "I liked her the second I met her!" or, "Just looking at him gave me the creeps!" Mimicry increases positive social behavior. Rick Van Baaren and colleagues at the University of Amsterdam have shown that individuals who have been mimicked are more helpful and generous not only toward their mimicker but also toward other people present than are nonmimicked individuals.25 Thus, when you mimic someone, it becomes more likely that this person will behave positively not only toward you but also toward other people around you, by fostering empathy, liking, and smooth interactions.26 This binding of people together through enhancing prosocial behavior may have adaptive value by acting as social glue that holds the group together25 and fosters safety in numbers. These behavioral consequences provide suggestive support for an evolutionary explanation of mimicry.

However, it is difficult to consciously mimic someone. Once we resort to conscious voluntary imitative behavior, we are just too slow. The whole conscious pathway takes too long. Muhammad Ali, whose motto was "Float like a b.u.t.terfly, sting like a bee," and who moved about as fast as anyone, took a minimum of 190 milliseconds to detect a light flash and another 40 milliseconds to begin his punch. In contrast, one study found that it took college students only 21 milliseconds to synchronize their movements unconsciously.27 Consciously trying to mimic someone usually backfires, looks phony, and throws the communication out of sync.

A few years back, Charlotte Smylie and I were able to work out which hemispheres of the brain are involved in voluntary and involuntary commands.28 Testing split-brain patients, we showed that while both hemispheres can respond to involuntary responses, only the left hemisphere can carry out voluntary responses. In addition, the left hemisphere uses two different neurological systems to carry out the voluntary, as opposed to the involuntary, responses. This is abundantly apparent when studying Parkinson's disease. This disease strikes the neurological system that controls the involuntary spontaneous facial responses. As a result, people suffering from Parkinson's disease don't show the normal facial reactions when engaged in social interactions. They might actually be having a good time, but because of their "mask," no one knows it. Parkinson's patients talk about this with great despair.

This tells us that physical action, such as mimicking facial expressions, is closely linked to the visual perception of the face, and happens so quickly and automatically that it seems there must be some closely linked neuronal pathways. But what is behind the action? There is a smile or a sneer, but what does that imply? Does the other person actually feel the emotion of the mimicked facial expression? Does this mimicry help us figure that out?

EMOTIONAL MIMICRY?.

If nonconscious automatic mimicry occurs with physical actions, does the same thing happen when observing emotional states? When I cut my finger, do you automatically copy how I am feeling and wince, or do you consciously reason it out? How about that shiver that you get up your spine? Do you consciously produce that, or is it an automatic response? If we automatically mimic a sad face (merely the physical action), do we actually feel sad, too? If we do feel the emotion, which comes first, the facial expression or the emotion? If we sense the emotion of the other, such as feeling sad, is it automatic? Or once we have the automatic sad face, do we consciously say to ourselves, "Gee, I seem to have this expression on my face that I remember I've had when I felt sad, and Sam has the same dang expression on his face, so I guess he must feel sad. I remember the last time I felt sad, and I didn't like that feeling and I bet he doesn't, either. Poor guy."

Do we consciously or unconsciously simulate the emotional states of others? If so, how do we do it, and how do we recognize which emotion it is? We need to be a bit careful here. I just casually threw in a word in the last paragraph that I wonder if you even noticed: feeling. Antonio Damasio has made a point of separating the definitions of emotion and feeling. He defines a feeling as "the perception of a certain state of the body (the emotion) along with the perception of a certain mode of thinking and of thoughts with certain themes." Your body can respond to a stimulus with an automatic emotion, but not until your conscious brain recognizes it can you say you have a feeling. He emphasizes the point that the emotion is what causes the feeling, not the other way around. This is contrary to the way most people think the brain works.29 EMOTIONAL CONTAGION.

Let's start with babies. How about when you go to the newborn nursery and all the babies are crying at once? Can it be that all of them are hungry and wet at the exact same time? No, not with all those nurses running around. Studies with newborns have shown that when they are exposed to the crying of another infant, a distress response is induced, and they will join in. However, when they hear their own cry that has been tape-recorded and played to them, or the cries of a baby several months older than they, or other random loud noises, a distress response is not induced, and they don't cry. The fact that babies are able to discriminate between their own cry and other infants' cries suggests that they have some innate understanding of the difference between themselves and others.30, 31 Is this a rudimentary expression of emotional contagion? That is the tendency to automatically mimic facial expressions, vocalizations, postures, and movements of another person and consequently to converge emotionally with them.27 It certainly seems to be, because if it were just a response to crying or loud noises in general, the newborn should cry even when he hears his own recorded cries, not just the cries of others. It also does not support theory theory, because then we would have to suppose the baby is thinking like this: "Aidan, Liam, and Seamus are crying in the ba.s.sinets all around me, and I know when I cry it is because I am hungry, wet, or thirsty, which, of course, is uncomfortable. Well, I feel fine, though. My diapers are dry, I just ate, and I am ready for a snooze.

But those guys must be miserable, just listen to them. I think I'll show a little baby solidarity and make a stink too." Perhaps a bit too sophisticated for a three-hour-old, who has not yet developed the ability to consciously recognize that others have separate beliefs and emotions.

Now consider this situation: You are laughing with a friend when the phone rings and she answers it. You are feeling great, you're sitting in the warm spring sun enjoying a steamy cappuccino, but now you look over at your friend's face, and you know something is dreadfully wrong. In a second, you no longer feel great, but anxious. You have caught her mood in a single glance.

An interesting experiment done by Roland Neumann and Fritz Strack, psychologists at the University of Wurzburg, Germany, demonstrates mood contagion. They were interested in finding out if a person who had no social motivation to interact with another person would still take on his mood. They also wanted to know if this was automatic or a result of taking the perspective of another. In order to figure this out, they had subjects listen to a tape recording of a rather dry philosophical text being read by an unknown person in a happy, sad, or neutral voice. Meanwhile, they also gave their research subjects a small physical task to do while they were listening. This was to divert their attention from the actual meaning of what was being read and the emotionality of the voice, so that wouldn't influence them. Then they were asked to read the same text out loud while they themselves were taped. The subjects not only automatically mimicked the tone of voice of the other person-happy, sad, or neutral-but what was even more interesting, they also took on the mood of the mimicked voice. They were also completely unable to recognize why they felt the way they did, and they hadn't realized that the voice they were mimicking had been happy or sad.32 So although there never was nor would be an actual social interaction, and the text that they were reading was not emotionally charged, and their attention to its content had been diverted, they still automatically mimicked the vocal tone and felt the same mood as the voice had indicated the reader was feeling.

These researchers define an emotion as having two components-a mood, and knowledge of why the mood is being felt. Mood is defined as the experience component itself, without the knowledge.

Neumann and Strack then did one further experiment. Up until this point, they had diverted the attention of the subject so that she had not noticed that the person whose voice she had been listening to had expressed an emotion. In this last experiment, they asked half of the subjects to adopt the perspective of the reader, with the idea that the subject would then consciously recognize the emotional component of the voice. Afterward, the subjects who had been directed to take the reader's perspective were able to identify that they had felt the emotion of sadness or happiness.

Infants Take On the Mood of Their Mothers.

Babies are affected by their depressed mothers. Studies of infant-mother pairs reveal that depressed mothers typically show flat affect, provide less stimulation, and respond less appropriately to their infant's actions. Their infants are less attentive, have fewer contented expressions, and are more fussy and less active33, 34 than babies with mothers who are not depressed. These infants are physiologically aroused by interactions with their depressed mothers: They have stress reactions, which are revealed by elevated heart rate and cortisol levels.35 They also appear to have a depressed mood, despite differences in the way their depressed mothers treated them.36 Unfortunately, these interactions can have long-term effects on these children.

Of course, the phenomenon of mood contagion should not come as a complete surprise to us. We come out of the grocery store laughing and feeling good after listening to the banter of a funny cashier, or when a smiling stranger nods at us. Living with a depressed roommate or family member puts a cloud on the whole household. One depressed, angry, or negative dinner guest can ruin a party, whereas a group of simpatico guests will spell its success. Moods are subtle and can be affected by a word or a painting or music. With knowledge about mood contagion, we can increase the frequency of good moods by putting ourselves in places "infected" with good moods so we can catch them! Such places include comedy clubs, bustling restaurants, funny movies, parks with kids having fun and laughing, colorful rooms, and outdoor locales with beautiful scenery. So moods and emotions appear to be automatically contagious. What is going on in the brain to make this happen?

Neural Mechanisms for Emotional Contagion?

Let's see if we can find out from neuroimaging studies how and why emotional contagion happens. Two emotional states that have been well studied in humans are disgust and pain-"yuck and ouch." These sound like excellent material for what we are interested in. Good thing there are psychology students! ("Hi, I'd like to volunteer for the disgusting experiment or, if that one is full, how about the pain one?") One group of volunteers watched a film of someone sniffing different fragrances, either disgusting ones, pleasant ones, or neutral ones, while their brain was being scanned with fMRI. Then they each had their turn at sniffing the same range of fragrances. It turned out that the same areas of the brain, the left anterior insula and the right anterior cingulate cortex, were automatically activated, both during the observation of disgusted facial expressions in the video and while experiencing the emotion of disgust evoked by the unpleasant fragrance. This suggests that the understanding of the facial expressions of disgust in someone else involves the activation of the same part of the brain that normally is activated during the experience of that same emotion.

The insula is busy in other ways, too. It also responds to gustatory stimulation: not just disgusting fragrances but disgusting tastes. Electrically stimulating the anterior insula during neurosurgery results in nausea or the sensation of being about to vomit,37 visceromotor activity (that queasy feeling you get), and unpleasant sensations in the throat and mouth.38 So the anterior insula partic.i.p.ates in transforming unpleasant sensory input, whether it is actual perception of the disgusting odor or flavor or merely observing someone else's facial reaction, into visceromotor reactions and the accompanying physical feeling one gets with the emotion of disgust.

So, at least for disgust, there is a common area in the brain that is activated for visually seeing the facial expression of the emotion in someone else, for one's own visceral response, and for feeling the emotion39-a tidy little brain package. The expression of disgust that you see on your wife's face when she sniffs the sour milk activates your own disgust emotion. Luckily, you don't need to sniff it yourself. Obviously this has an evolutionary advantage. Your companion takes a bite of the rotting gazelle carca.s.s and makes the disgust face. Now you don't have to test it. Interestingly, the same did not hold true for the pleasant fragrance. Pleasant fragrances activate the posterior right insula only, and we know we don't get the same visceromotor response.

Pain also appears to be a shared experience. In the movie Marathon Man, we all cringed at the dental torture scene. In our brains, there is an area that responds to both the observation of pain and the experience of pain. Volunteer couples were scanned with fMRI while one was being given a painful shock to the hand and the other was an observer. There are anatomical connections between regions that make up the pain system in the brain; these do not function independently but are highly interactive. However, there appears to be a separation between the sensory ("that hurts!") and emotional perceptions of pain, such as its antic.i.p.ation and the anxiety that it produces ("I know it's going to hurt, oh, hurry up and get it over with, ohhh, when is it going to happen?"). What the scans showed was that both the observer and the recipient of pain had activity in the part of the brain that is active with the emotional perception of pain,* but only the recipient had activity in the area that is active with the sensory experience,40 which is a good thing. You wouldn't want the paramedic himself to need to be anesthetized while he was stabilizing your broken femur, but you do want him to be gentle with your painful leg: You want him to realize it hurts but not to feel it himself to the point of inaction.

Clearly, whether you antic.i.p.ate the pain for yourself or another, the same area in the brain is used. Looking at pictures of humans in painful situations also activates brain activity in the area that is active in the emotional appraisal of pain, but not the area that is active with the actual sensation of pain.41 There is evidence the same neurons mediate the emotional appraisal of both personal and vicarious pain. In rare cases, patients who have had portions of their cingulate removed have had testing of neurons under local anesthesia with microelectrodes. This has shown that the same neuron in the anterior cingulate fired upon experiencing a painful stimulus and also while antic.i.p.ating or observing one.42 This indicates that the observation of an emotion in someone else can result in brain activity that matches the experience of the emotion, to a certain degree, automatically.

These findings have very interesting implications for the emotion of empathy. Without going into a long discussion of the definition of empathy, we can at least agree that it implies being able to detect accurately the emotional information being transmitted by another person, being conscious of it, and caring about it. To care about another's state is an altruistic behavior, but it cannot occur without good information. If I cannot accurately detect your emotion, if I think that you are disgusted when in fact you are in pain, I will react to you inappropriately, perhaps handing you a Compazine suppository instead of Advil.

Tania Singer and colleagues at the University College London, who did the pain research with the couples, wondered, as you may too, if observers who had higher pain-related brain activity were more empathetic. So they gave the couples a standardized test that rates emotional empathy and empathetic concern. Indeed, the individuals who scored higher on general empathy scales did show stronger brain activity in the portions of the brain that were active when they perceived their partner as being in pain. There was also a correlation between how empathetic one rated oneself and how much activity there was in the anterior rostral zone of the cingulate, an area near the center of the brain. Also in the second study, when people looked at pictures of painful situations, the activity in the anterior cingulate was strongly correlated with their ratings of the others' pain. The more activity, the higher they rated the pain, suggesting that the activity of this brain region varies according to subjects' reactivity to the pain of others.

The work on disgust and pain suggests that the simulation of these emotions is automatic. The question remains whether the simulation of the emotion comes first and then the automatic physical mimicry follows, or the automatic mimicry is followed by the emotion. When you see your wife's face after she sniffs the sour milk, do you automatically copy her expression, and then feel the disgust, or do you see her facial expression of disgust, feel disgust yourself, and then automatically make the disgust face? The chicken-and-egg problem continues to be unresolved in this particular case.

PHYSIOLOGICAL SIMULATION.

When you feel a negative emotion, such as fear, anger, or pain, you also get a physiological response, just as babies have a stress response to hearing other newborns crying or when interacting with a depressed mother. Your heart races and you may sweat or get the shiver up your back, and so forth. In fact, you get a different set of physiological responses with each different emotion.43, 44 They are emotion-specific. Would your physiological response to an observed situation be able to predict how accurately you interpreted the emotion of the other person? If your physiological response were more similar to the other person's, would you be better at judging her emotion?

That is what Robert Levenson and colleagues at the University of California, Berkeley, demonstrated happens for negative emotions. They measured five physiological variables* in subjects as they watched four separate videotaped conversations between married couples. These same measurements had been taken of the couples as they were having the conversations. Throughout the conversations, the subjects a.s.sessed what they thought the husband or the wife was feeling. The subjects whose autonomic physiological responses more closely simulated those of the person they were observing did indeed interpret his or her negative emotions more accurately. This did not hold true for positive emotions. These results suggest a relation between physiological linkage (how closely one simulates the physiological response) and rating accuracy for negative emotions. The researchers suggest that empathetic subjects (i.e., those who are most accurate in rating the negative emotions of targets) would be most likely to experience the same negative emotions. These negative emotions would produce similar patterns of autonomic activation in both subject and target, thus resulting in high levels of physiological linkage.45 The other question this presents is, "Do people who are more sensitive to their physiological responses have more intense emotional feelings? If I am acutely aware (conscious) that my heart is beating faster and I am sweating, am I more anxious or scared than someone who doesn't notice? If I pay more attention to my physiological responses, am I more empathetic to others?"

Hugo Critchley and colleagues at Brighton and Suss.e.x Medical School, England, provided the answer to this question and also found out a little bonus information.46 They gave a group of people a questionnaire that rated symptoms of anxiety, depression, and positive and negative emotional experience. None of the subjects scored in the range necessary for a diagnosis of either depression or anxiety. Then they were scanned with fMRI while judging whether an auditory feedback signal, a repeated musical note, was synchronous with their heartbeat or not. This measured their attention to a physiological process-their heartbeat. They were also asked to listen to a series of notes and distinguish which one was a different tone. This was to test their perception, how well they could distinguish differences in sensory input. This separates how intensely one feels a pain (perception) from how intensely one focuses on it (attention).

The researchers also measured the size of the activated brain regions. They found that activity in the right anterior insular and opercular cortex predicted subjects' accuracy in detecting (attention) their heartbeat. And the size of that particular portion of the brain itself mattered! The larger it was, the more accurate the person was at detecting their internal physiological state, and these same people also had higher self-ratings of body awareness. However, not everyone who had rated themselves high in body awareness was actually good at detecting their heartbeat. This was that old problem of people thinking they are better at something than they are. With one exception, those who were actually good at detecting their heartbeat were only those with a greater volume of that particular brain area: big right anterior insula, more body self-awareness, more empathy. The exception was that subjects who had scored higher in past negative emotional experiences also had increased accuracy in detecting their heartbeat.

These findings indicate that the right anterior insula is involved with visceral responses that can be recognized (which we already learned from the disgust experiments) and that recognizing these responses can lead to subjective feelings. Some people are better at recognizing these internal signals than others. Some people are just born that way with a larger insula, but also some have acquired the ability by having had more negative experiences in their past. These results may explain why some people are more aware of their feelings than others.47 PAIRED DEFICITS.

The above findings, coupled with the findings that increased neural activity a.s.sociated with the emotional component of pain increases empathy, make one wonder: If one can't feel an emotion (no brain activity, no physiological response), can one recognize it in someone else? This questions one of the main tenets of simulation theory-that we simulate the other person's state of mind and then, from our own personal experience of that state of mind, we predict how the other is feeling or what his behavior will be. Is this true? Are there paired deficits? If a person has a lesion in their insula, do they neither feel nor recognize disgust? If nothing disgusts me, can I recognize disgust in you? What if there is a lesion in the amygdala, what does that do? If we look at people who have a brain lesion that affects a particular emotion, does it change their ability to detect that emotion in another?

These paired deficits have indeed been shown to exist. Andrew Calder and colleagues at Cambridge University tested a patient with Huntington's disease who had damage to his insula and putamen. They hypothesized that because the insula has been shown in neuroimaging studies to be involved with the emotion of disgust, their patient should be limited in his ability to recognize disgust in others and also should have less of a disgust reaction himself. This turned out to be true. He didn't recognize disgust from facial signals or from verbal signals, such as retching, and he was less disgusted than controls by disgust-provoking scenarios.48 Ralph Adolphs and colleagues at Caltech and the University of Iowa had a patient with a rare bilateral insula lesion. He was unable to recognize disgust in facial expressions, actions, descriptions of actions, or pictures of disgusting things. When he was told a story about a person vomiting, then asked how that person would feel, he said they would be "hungry" and "delighted." After observing someone act out vomiting unpalatable food, he said, "Delicious food was being enjoyed." He could not recognize disgust in others, nor did he appear to feel the emotion of disgust. He is reported to eat indiscriminately, including items that are not edible, and he "fails to show any disgust to food-related stimuli, such as pictures of food covered with c.o.c.kroaches."49 Remember from the last chapter that disgust appears to be a uniquely human emotion.

Now back to the amygdala. We just learned that the amygdala is part of the pain system, but we have seen in a previous chapter that it is also concerned with fear. Adolphs and his team have found that people with right hemisphere lesions to their amygdala have impaired recognition of various negative facial expressions, including fear, anger, and sadness, but people with lesions to the left hemisphere amygdala are able to recognize these expressions. Amygdala lesions did not affect the ability to recognize happy expressions.50 Patients with bilateral lesions of the amygdala (although it is the damage to the right side that is causing the problem) appear to have selective impairment in interpreting fearful expressions.50, 51, 52 In a group of nine patients with bilateral amygdala damage (there are very few people with lesions like this), although they intellectually understood what should be a frightening situation (a car coming at them, confronting a violent person, illness and death), they could not recognize fear in the facial expressions of others.53 In a different study, a patient with bilateral amygdala damage did not recognize fear in the facial expressions, emotional sounds, or posture of others. His own everyday experience of both the emotions of anger (an emotion he had no problem in recognizing in others) and fear were reduced, compared with neurologically normal controls. His low fear level allowed him to engage in such activities as jaguar hunting in the Amazon River basin and hunting while hanging from a helicopter in Siberia.54 These patients have shown us that not perceiving the emotion and not feeling the emotion are linked, and they suggest that a neural lesion preventing one from feeling or simulating an emotion may also prevent one from recognizing it in others.

And what about patient X, the blind stroke victim who can guess emotional facial expressions? When he was scanned with fMRI while doing so, his right amygdala became active.1 Remember when we learned about the fast-track pathway for fear, whereby incoming information goes to the thalamus and then straight to the amygdala? That is what is happening with patient X. The visual stimuli can still go to the amygdala even if the connection to the visual cortex has been disrupted, and the amygdala still does its job. The amygdala is not connected to the speech center. It does not tell the speech center, "I just saw a really scared face," so patient X can guess that the photo being presented to him is of a scared person. Instead, the amygdala creates a feeling. Patient X is automatically simulating a feeling; then he can guess the expression based on how he is feeling. He did not need the conscious brain to recognize the emotion!

All this talk about activating areas in the brain is actually referring to the fact that a neurochemical process is going on in that region. Another way to investigate emotion recognition is to artificially block an emotion with a drug that suppresses it, and then see if the subject can recognize the emotion in someone else. This was done in a study of anger recognition. One form of human aggression occurs over disputes about property or dominance, and it is a.s.sociated with the facial expression of anger. Your neighbor thinks the strip of property between your driveways is his; you think it is yours. He gets mad when he sees you have dug it up and planted roses, so he digs them up. You get mad.

Andrew Lawrence, Trevor Robbins, and colleagues at Cambridge postulated that a separate neural system might have evolved specifically to recognize and respond to this specific threat or challenge. In many animals, it has been shown that increased attention to these types of aggressive encounters is a.s.sociated with the body producing increased levels of the neurotransmitter dopamine. If an animal is given a drug that blocks the action of dopamine, this impairs the reactions to these types of encounters but does not affect its locomotion-so if it doesn't react to an aggressive act, you know it isn't because it can't move. You could still chainsaw your neighbor's prize sycamore tree that drops leaves all over your lawn, but you don't. They wondered if blocking the dopamine would not only decrease the reaction to anger expressions but also decrease the recognition of anger expressions.

This is indeed what happened. "Why, Fred, by golly, you seem to have dug up my roses. What about those Sox anyway?" Even more interesting, there was no effect on the ability to recognize all other emotions. "By the way, your wife is looking at you with a rather disgusted expression, what's up with her?" The implications of a distinct system for the processing of specific emotional signals (e.g., fear, disgust, and anger) support psycho-evolutionary approaches to emotion. They suggest that distinct systems may have evolved for these negative emotions in order to detect and coordinate flexible responses to different ecological threats or challenges.55 DO OTHER ANIMALS SIMULATE BEHAVIOR AND EMOTIONS?.

There is evidence for a similar type of automatic emotional simulation in nonhuman primates. Emotional mimicry has been identified in the lab with monkeys. And just as with humans, damage to the amygdala in macaque monkeys results in monkeys with reduced fear and aggression and increased submissiveness.56 They were tamer and abnormally friendly. If these monkeys also simulated emotions, and the amygdala has a role in their emotion of fear similar to its role in humans, then you would expect that parts of their amygdala would be active when they viewed another individual with a fearful expression. Single-neuron studies have shown that this occurs. Emotional contagion is evident in monkeys. It has also been shown in rats and pigeons. So emotional contagion is not unique to humans. Many researchers think it is the foundation stone necessary for the more highly evolved emotion of empathy, which requires consciousness and altruistic caring.

The question as to whether empathy is a uniquely human emotion, or whether other animals share it, is actively being researched, with partisans in both camps. Everyone agrees that the extent of human empathy far surpa.s.ses its extent in other animals. Studies have shown that rats that have been trained to press a bar for food will stop pressing it if another visible rat gets a shock when the lever is pressed.57 Various permutations of such tests have been done, but the basic question remains. Does the rat stop pressing the bar because of altruistic, empathetic impulses, or does he stop because the experience of seeing another rat being shocked is unpleasant? The difference is between a response to a visually perceived unpleasantness versus all that const.i.tutes empathy: theory of mind, self-awareness, and altruism. This dilemma also plagues other studies that have been done with rhesus monkeys. Tests have yet to be designed that convincingly tease these two responses apart.

Another avenue of exploration is chimpanzee yawning. In a group of chimps, one-third will yawn while watching videos of other chimps yawning.58 Some 40 to 60 percent of people will yawn while watching videos of yawning. I am yawning right now. It has been suggested that contagious yawning may be a primitive form of empathy. Steve Platec and colleagues suggest that, rather than just being an imitative action, it uses parts of the brain that are a.s.sociated with theory of mind and self-awareness.59 He found that people who were more susceptible to contagious yawning also could identify their own face faster and do better on theory-of-mind tasks. He has evidence from neural imaging that supports this idea.60 Humans' empathetic behavior far surpa.s.ses contagious yawning, of course. It is no surprise that we have discovered some foundational behavior in the chimps, but so far, evidence for the altruistic, conscious empathy that humans possess is elusive in other animals.

MIRROR NEURONS AGAIN.

How does the brain link observation of a facial expression with the action of copying it? How does it link facial expressions with particular emotions? You may already have started to wonder about those mirror neurons again. Those puppies are important! The first concrete evidence that perhaps there was a neural link between observation and imitation of an action was the discovery of mirror neurons, which we talked about in chapters 1 and 2. If you recall, the same premotor neurons fired both when a macaque monkey observed others manipulating an object, such as by grasping, tearing, or holding it, and when it executed the action itself. Mirror neurons for hearing have also been found in monkeys, so that the sound of an action in the dark, such as ripping paper, activates both these auditory mirror neurons and the action neurons for the action of ripping paper.61 We already have learned that since that time, several studies have shown the existence of a similar mirror system in humans. For instance, a group of subjects were studied with an fMRI scanner, either while they merely watched a finger being lifted, or while they watched and then copied the movement. The same cortical network in the premotor cortex was active in both conditions, just watching, or watching and doing, but it was more active in the second condition.62 In humans, the mirror system is not restricted to hand movements but has areas that correspond to movements all over the body. There is also a difference when there is an object involved in the action. Whenever an object is the target of action, another area of the brain (the parietal lobe) is also involved. A specific area will be active if a hand is using an object, such as lifting a cup, and a different area will be active if the mouth is acting on an object, perhaps sucking on a straw.63 It is not possible to locate individual mirror neurons in humans as it is in the monkey, owing to the type of testing procedures. However, mirror neuron systems have been found in several areas of the human brain.

There is a distinct difference, however, between the mirror neurons in the monkey and the systems we humans have. The mirror neurons in the monkey fire only when there is goal-directed action, such as when they see a hand grasp an ice cream cone and move it to the mouth, which happened to be the case when the first mirror neurons were seen firing (although it was actually a gelato). In humans, however, the mirror system fires even when there is no goal.64 A hand randomly waving in the air will cause the system to activate. This may explain why, although monkeys have mirror neurons, there is very limited imitation. The monkey's mirror system is tuned to the goal and does not code all the details of the action leading to the goal.65 The prefrontal lobe also plays an important role in imitation,66 and humans, with their larger prefrontal cortex, may just have the advantage over monkeys by being able to build more complex motor patterns. We can watch someone play a guitar chord, and copy it movement for movement. We can take dance lessons and imitate our instructor as he sambas across the floor. A monkey would understand only that we went to the other side of the room, not that gyrating was necessary. The fact that monkeys have a less complex system helps us understand the evolutionary development of the mirror neuron system. Giacomo Rizzolatti and Vittorio Gallese originally proposed that the function of the mirror neuron system was to understand action (I understand that a cup is being lifted to the mouth). This action understanding is present in both monkeys and humans. However, in humans, the mirror neuron system is capable of doing much more. Are humans unique because they are the only animal that can samba?

What all are the mirror systems involved in? As we saw above, they are involved with immediately copying actions. It has also been found that they are involved with understanding why the action is being done, its intention.67 I understand that a cup is being lifted to the mouth (the action understanding of the goal) to see how its contents taste (the intention behind the action). The same action is coded differently if it is a.s.sociated with different intentions, thereby predicting the likely future un.o.bserved action. In monkeys, a different set of mirror neurons activates if food is grabbed to be lifted to the mouth, or to be put in a cup. (I understand that the food is being grabbed to be eaten versus being grabbed to be put in a cup.) Not only do you understand someone is grabbing a candy bar, you understand she is going to eat it or put it in her purse or throw it out or, if you're lucky, hand it to you.

Are there mirror neurons for understanding emotion, too, or are they just for physical actions? The findings that we discussed above of the paired deficits in feeling and recognizing disgust and pain are suggestive that there are mirror systems located in the insula, which, as in action understanding, are involved with emotion observation and with understanding mediated through the visceromotor response.68 The theory that mirror neurons are involved in emotion observation and understanding (which contributes to social skills) has led two groups of researchers* to suggest that some of the symptoms of autism may be caused by a defect in the mirror-neuron system. These symptoms include lack of social skills, lack of empathy, poor imitation, and language deficits. Although Rizzolatti used electrodes to study mirror neurons in monkeys, researchers in San Diego have come up with a way to test for mirror neurons in humans without using electrodes.69 One of the components of EEGs, the mu waves, are blocked when a person makes a voluntary muscle movement and also when one watches the same action. The University of California, San Diego, group decided to see if EEGs could monitor mirror-neuron activity. They studied ten children with high-functioning autism and found they did suppress mu waves when they performed an action, just as normal children did, but unlike normal children, they did not suppress the mu waves when they observed an action. Their mirror system was deficient.

Another study70 was done at UCLA, where children (both normal and with autistic spectrum disorder, ASD) were scanned using fMRI while either observing or imitating emotional facial expressions. Because individuals with ASD often show deficits in understanding the emotional states of others, it was predicted that dysfunction in the mirror-neuron system (MNS) should be manifest both when these individuals imitate emotional expressions and when they observe emotions displayed by others. This prediction proved correct. Moreover, the degree of reduction in neural activity correlates with the severity of deficit in social skills. The less activity, the less socially skilled they were.

The two sets of children use different neural systems when imitating facial expressions. The normal children use a mirroring neural mechanism in the right hemisphere that links with the limbic system via the insula. However, this mirroring mechanism is not engaged in children with ASD, who adopt a different strategy. They increase their visual and motor attention, using a pathway that does not go through the limbic system and the insula. The internally felt emotion of the imitated facial expression regulated by the insula is probably not experienced. These researchers suggest that because both adults and normally developing children show increased MNS activity even when simply observing an emotional expression, this is more proof that the mirroring mechanism may underlie the remarkable ability to read others' emotional states from facial expressions. The lack of MNS activity in children with ASD strongly supports the theory that dysfunction in the mirror-neuron system may be at the core of the social deficits observed in autism. However, there are many nonsocial attention skills that are also impaired in autism; they may not be involved with the mirror-neuron system.

It is currently unknown if animals other than primates have mirror-neuron systems, but it is being checked out. However, just as Clint Eastwood said, "A man's got to know his limitations."71 We need to understand the limitations of the mirror neurons. They do not generate actions.

So far we have seen that specific emotions are a.s.sociated with activity in specific parts of the brain, and specific physiological responses and specific movements of the facial muscles result in specific expressions. When we perceive another individual exhibiting some type of mood or emotion, we automatically mimic it, both physiologically and physically, and psychologically to some extent. If there is some abnormality in the brain structure that normally supports the response, then both the ability to experience the emotion and the ability to recognize it in others are affected. We have a mirror system that understands actions and the intentions of actions, and it is also involved with learning through imitation and emotion recognition. This is Emotion Recognition 1-elementary emotion recognition. It seems as though we have built up a good case for some type of simulation going on from one person to the next.

MORE THAN AUTOMATIC?.

Even though this a.n.a.lysis looks reasonable, there is a wrench in the machinery. People who have Mobius syndrome (congenital facial paralysis due to the absence or underdevelopment of the cranial nerves that supply the facial muscles) can successfully identify emotions in the faces of others, even though they are not able to physically mimic facial expressions.72 This may not be a problem if our understanding of emotions is via the mirror neurons. They may still fire, even though the motor system is not functioning.

Another wrench is a recent study on subjects who have a congenital inability to feel pain (CIP). From facial expressions, these people are able to recognize and rate the pain that others feel just as well as normal controls, even though they themselves feel none. If, however, they are presented with video clips in the absence of visible or audible pain-related behavior, CIP patients rate the pain as lower, and they have less aversive emotional responses, compared with control subjects.

One additional interesting finding is that pain judgments in CIP patients are strongly related to individual differences in emotional empathy, and this correlation is not found in control subjects. The authors of this study suggest that personal experience of pain is not necessarily required for perceiving and feeling empathy for another's pain, although it might be greatly underestimated when there are no emotional cues.73 However, in both cases, the patients with Mobius syndrome and CIP have had long-standing deficits. Their ability to recognize emotions in others may have been consciously learned over the years via a different pathway than that in normal subjects. The authors note that the parents of some CIP patients may resort to miming facial expressions of pain to make their child understand that a particular stimulus might damage his body.

We have learned that watching or hearing other individuals in pain activates some of the cortical areas known to be involved in the emotional component of self-pain experience, such as the anterior cingulate cortex and the anterior insula. In contrast with the neural mechanism for actually feeling pain, mirror matching of the emotional aspect of another's pain might be preserved in CIP patients. Thus they could detect suffering in others from emotional cues such as facial pain expressions. At the end of this study, one-third of the patients said that they found it difficult to estimate the pain experienced by injured individuals without seeing their face or hearing them cry. Scanning these patients during these emotional recognition tasks to see what neural areas are being used would be interesting, as well as timing their responses compared to those of normal subjects. Is it a slower conscious pathway that is used, or is it a fast automatic one?

Another finding that indicates automatic simulation is not all that is going on came from a study done by Ursula Hess and Silvie Blairy at the University of Colorado. They found that the occurrence of mimicry did not correlate with the accuracy in facial emotional recognition.74 This study used facial expressions that were not exaggerated but were thought to be more like those one usually experiences. So even though facial mimicry did occur, it did not correlate with the accurate diagnosis of the emotion being felt by the observed person. Other studies have shown that people do not mimic the faces of those with whom they are in compet.i.tion75 or of politicians with whom they do not agree.76 Is some inhibitory ability going on? It seems there must be, otherwise we would start crying in the baby nursery with all the newborns. Is some voluntary cognition involved?

I THINK, THEREFORE I CAN REAPPRAISE.

Indeed we can change our emotion and the way we feel by the way we think. One way this is accomplished is by reappraisal. This is what happened to Modeste Mignon, our fictional example in the last chapter. "In love, what a woman mistakes for disgust is simply seeing clearly." After a reappraisal of her lover's character, she goes from love to disgust.77 A car cuts in front of you and zooms down the street. It makes you angry. As your blood pressure starts to rise, all of a sudden you remember when you did the same thing on a terrifying drive to the emergency room. Next to you was your child whimpering in pain with a dislocated shoulder hanging at his side. Your anger dissipates in a second, your blood pressure drops, and now you feel concern as you realize the hospital is down the road.

Conscious reappraisal of an emotion has been investigated in a brain imaging study where partic.i.p.ants were presented with photos showing negative but somewhat ambiguous emotional situations, such as a woman crying outside of a church. While being scanned, the subjects were then asked to reappraise the situation in a more positive way. The thought was that reappraisal draws attention to the emotion one is feeling and requires a voluntary cognitive a.s.sessment. After reappraisal, such as imagining that the woman was shedding tears of joy after a wedding, versus their initial impression of a funeral scene, the partic.i.p.ants reported being less negatively affected. The scanning results showed that during reappraisal, there was decreased activity in regions concerned with emotional processing, and activation in regions that are essential for memory, cognitive control, and self-monitoring.78 Reappraisal can modulate emotion and simulation. Another interesting finding was that the left hemisphere was more active in reappraisal. It is theorized that perhaps this may be because partic.i.p.ants reported having "talked" themselves into reappraisal strategies, and the speech center is in the left hemisphere. Another possible explanation is that the left hemisphere is known to be a.s.sociated with evaluating positive emotions in general.79 People who show a higher resting activity of the left hemisphere have more resistance to depression, which may be because of their cognitive ability to decrease negative emotional processing.

SUPPRESSION.

Another way simulation can be affected is through suppression, that is, voluntarily not showing any sign of an emotion. Parents often do this when they don't laugh at their child's funny but inappropriate social behavior (pulling off her dirty diapers in the pool), although it can be difficult. In a review of research on emotional regulation,80 James Gross of Stanford University explains that suppression requires one to continually monitor one's expressions (that smile might just pop back up) and correct them (if it does). This is using your conscious neural circuits, which we have learned are limited, and it takes your conscious attention away from the social interaction. This leaves you with less ability to process the interaction and can affect your memory of it. This is different from when you reappraise a situation and you no longer actually feel the emotion, so there is no need to monitor to make sure it doesn't show. (Pulling off her dirty diapers in the swimming pool actually isn't funny, it is disgusting: There is no chance of the smile creeping back.) Suppression and reappraisal have different emotional, physiological, and behavioral consequences. Suppression does not decrease the emotional experience of negative behavior; you still have the emotion, you just don't express it. When the car cuts you off in traffic, you may not scowl at the driver and ram his b.u.mper, but you are still angry. This is unlike reappraisal, when you realized the other driver might need the hospital services and you no longer felt the emotion of anger. However, suppression can decrease the emotional experience of positive behavior. Great, that is par for the course. You try to suppress bad emotions, and not only doesn't it get rid of them, but now you don't feel the good ones as well. Nor does suppression change the physiological responses. You still get all the increased cardiovascular activity. You may be hiding your anger, disgust, or fear, but you're still making your heart work overtime and wearing it out that much sooner. However, reappraisal can change the physiological response; it can decrease the stress of a stressing situation. If you can change your att.i.tude about a negative stimulus so that it is no longer negative, then you won't be borrowing unnecessarily from your cardiovascular bank account.

How does this affect simulation? The interesting consequence of suppressing emotional expressions is that it hides important signals that would otherwise be available to the other person in a social situation. She is talking to old stone face, has no clue how he is feeling, and so can't respond to him appropriately. And lord knows he isn't going to respond to her. She has just told him her funniest story, and he is looking at her as if she should never have graduated from elementary school. She reminds herself to put him on the "do not invite" list, to spare her friends this trying social interaction. And how about old stone face? His social interactions will be limited, for no doubt she is not the only one to avoid him.

Researchers studying suppression with James Gross made a prediction: Because one needs to monitor oneself while suppressing an emotion to be sure the expression isn't popping up visibly or vocally, then one may be distracted from actually responding to the other's emotional cues. This could have negative social consequences. If a person is focused on himself, there is less conscious focus available for another person. The guy trying to act macho all the time has to suppress any tender expressions that may be trying to erupt. He has less available brain capacity to be paying attention to anyone interacting with him. Gross and his colleagues also thought that since reappraisal isn't so cognitively taxing, it should have more positive social consequences.

They set out to test this theory by asking unacquainted women to watch an upsetting film and then discuss it afterward. One woman in each couple had been asked to do one of three things. She was to suppress her reactions to the film (as a macho guy may do: "I'm tough, those gory pictures mean nothing to me"), or reappraise ("Those pictures are awful, but it is only a movie, and that is really ketchup"), or interact naturally with her conversation partner. The other woman did not know that any instructions had been given to her partner. Their physiological responses were measured during the conversations.

Positive expressions of emotion ("That is so great!! I'm so excited for you!") and emotional responsiveness ("Oh brother, that must drive you crazy; it would me!") are key elements in social support, which decreases stress.81 The researchers figured if this social support was absent, then there should be a big difference in the physiological responses to the conversations among the group of the uninformed partners. This proved true. The conversation partners of the women who had been told to suppress had greater increases of blood pressure than the women whose partners either acted naturally or had reappraised the film.82 Interacting with people who express little positive emotion and who are unresponsive to emotional cues actually increases the cardiovascular activity in their social partners.80 So if you hang out with someone who suppresses his expressions of emotion, it not only makes his blood pressure go up, it makes yours go up too.

Things are getting a little more complicated now. It seems that we have gone beyond a world of emotional contagion, where simulation is a reflexive automatic response to facial expressions or other emotional stimuli, and entered into the world where the conscious brain plays a role. Here you a